Abstract
Vertebrate gastrulation involves the specification and coordinated movement of large populations of cells that give rise to the ectodermal, mesodermal and endodermal germ layers. Although many of the genes involved in the specification of cell identity during this process have been identified, little is known of the genes that coordinate cell movement. Here we show that the zebrafish silberblick (slb) locus1 encodes Wnt11 and that Slb/Wnt11 activity is required for cells to undergo correct convergent extension movements during gastrulation. In the absence of Slb/Wnt11 function, abnormal extension of axial tissue results in cyclopia and other midline defects in the head2. The requirement for Slb/Wnt11 is cell non-autonomous, and our results indicate that the correct extension of axial tissue is at least partly dependent on medio-lateral cell intercalation in paraxial tissue. We also show that the slb phenotype is rescued by a truncated form of Dishevelled that does not signal through the canonical Wnt pathway3, suggesting that, as in flies4, Wnt signalling might mediate morphogenetic events through a divergent signal transduction cascade. Our results provide genetic and experimental evidence that Wnt activity in lateral tissues has a crucial role in driving the convergent extension movements underlying vertebrate gastrulation.
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References
Heisenberg,C. P. et al. Genes involved in forebrain development in the zebrafish, Danio rerio. Development 123, 191– 203 (1996).
Heisenberg,C. P. & Nüsslein-Volhard,C. The function of silberblick in the positioning of the eye anlage in the zebrafish embryo. Dev. Biol. 184, 85 –94 (1997).
Tada,M. & Smith,J. C. Xwnt11, a target of Xenopus Brachyury: Regulation of gastrulation movements via Dishevelled, but not through the canonical Wnt pathway. Development (in the press).
Boutros,M. & Mlodzik,M. Dishevelled: at the crossroads of divergent intracellular signaling pathways. Mech. Dev. 83, 27–37 (1999).
Warga,R. M. & Kimmel,C. B. Cell movements during epiboly and gastrulation in zebrafish. Development 108, 569–580 (1990).
Keller,R., Shih,J. & Domingo,C. The patterning and functioning of protrusive activity during convergence and extension of the Xenopus organiser. Development (Suppl.), 81–91 (1992).
Hammerschmidt,M. et al. Mutations affecting morphogenesis during gastrulation and tail formation in the zebrafish, Danio rerio. Development 123, 143–151 ( 1996).
Solnica-Krezel,L. et al. Mutations affecting cell fates and cellular rearrangements during gastrulation in zebrafish. Development 123, 67–80 (1996).
Moon,R. T. et al. Xwnt-5A: a maternal Wnt that affects morphogenetic movements after overexpression in embryos of Xenopus laevis. Development 119, 97–111 ( 1993).
Du,S. J., Purcell,S. M., Christian, J. L., McGrew,L. L. & Moon,R. T. Identification of distinct classes and functional domains of Wnts through expression of wild-type and chimeric proteins in Xenopus embryos. Mol. Cell. Biol. 15, 2625–2634 (1995).
Ungar,A. R., Kelly,G. M. & Moon,R. T. Wnt4 affects morphogenesis when misexpressed in the zebrafish embryo. Mech. Dev. 52, 153– 164 (1995).
Makita,R., Mizuno,T., Koshida,S., Kuroiwa,A. & Takeda,H. Zebrafish Wnt11—pattern and regulation of the expression by the yolk cell and no tail activity. Mech. Dev. 71 , 165–176 (1998).
Cadigan,K. M. & Nusse,R. Wnt signaling—a common theme in animal development. Genes Dev. 11, 3286 –3305 (1997).
Moon,R. T. & Kimelman,D. From cortical rotation to organizer gene expression—toward a molecular explanation of axis specification in Xenopus. BioEssays 20, 536– 545 (1998).
Glinka,A., Wu,W., Onichtchouk,D., Blumenstock,C. & Niehrs, C. Head induction by simultaneous repression of Bmp and Wnt signalling in Xenopus. Nature 389, 517–519 (1997).
Pai,L. M., Orsulic,S., Bejsovec,A. & Peifer,M. Negative regulation of Armadillo, a wingless effector in Drosophila. Development 124, 2255–2266 ( 1997).
Pelegri,F. & Maischein,H. M. Function of zebrafish beta-catenin and Tcf-3 in dorsoventral patterning. Mech. Dev. 77 , 63–74 (1998).
Molenaar,M. et al. Xtcf-3 transcription factor mediates beta-catenin-induced axis formation in Xenopus embryos. Cell 86, 391–399 (1996).
Axelrod,J. D., Miller,J. R., Shulman,J. M., Moon,R. T. & Perrimon,N. Differential recruitment of dishevelled provides signaling specificity in the planar cell polarity and Wingless signaling pathways. Genes Dev. 12, 2610– 2622 (1998).
Wilson,P. A., Oster,G. & Keller,R. Cell rearrangement and segmentation in Xenopus: direct observation of cultured explants. Development 105, 155 –166 (1989).
Saude,L., Woolley,K., Martin,P., Driever,W. & Stemple, D. L. Axis inducing activity and cell fates of the zebrafish organizer. Development (submitted).
Boutros,M., Paricio,N., Strutt,D. I. & Mlodzik,M. Dishevelled activates JNK and discriminates between JNK pathways in planar polarity and wingless signaling. Cell 94, 109– 118 (1998).
Kimmel,C. B., Warga,R. M. & Kane,D. A. Cell cycles and clonal strings during formation of the zebrafish central nervous system. Development 120, 265–276 (1994).
Elul,T., Koehl,M. A. & Keller, R. E. Cellular mechanisms underlying neural convergent extension in Xenopus laevis embryos. Dev. Biol. 191, 243–258 (1997).
Rauch,G.-J., Granato,M. & Haffter, P. A polymorphic zebrafish line for genetic mapping using SSLPs on high-percentage agarose gels. Tech. Tips Online T01208 (cited 080300) 〈http://www.biomednet.com/db/tto〉 ( 1997).
Knapik,E. W. et al. A reference cross DNA panel for zebrafish (Danio rerio ) anchored with simple sequence length polymorphisms. Development 123, 451–460 ( 1996).
Barth,K. A. & Wilson,S. W. Expression of zebrafish nkx2.2 is influenced by sonic hedgehog/vertebrate hedgehog-1 and demarcates a zone of neuronal differentiation in the embryonic forebrain. Development 121, 1755–1768 (1995).
Concha,M. L. & Adams,R. J. Oriented cell divisions and cellular morphogenesis in the zebrafish gastrula and neurula: a time-lapse analysis. Development 125, 983–994 (1998).
Yamamoto,A. et al. Zebrafish paraxial protocadherin is a downstream target of spadetail involved in morphogenesis of gastrula mesoderm. Development 125, 3389–3397 (1998).
Kobayashi,M., Toyama,R., Takeda,H., Dawid,I. B. & Kawakami, K. Overexpression of the forebrain-specific homeobox gene six3 induces rostral forebrain enlargement in zebrafish. Development 125, 2973–2982 ( 1998).
Acknowledgements
We thank T. Schilling, C. Houart, P. Haramis and F. Conlon for critical reading of this manuscript, many colleagues for providing reagents, and the late P. Haffter for providing data before publication. C.P.H. and M.L.C. were supported by postdoctoral fellowships from EMBO, the EC and the Wellcome Trust. G.J.R. and R.E.G. were supported by a grant from the German Human Genome Project. L.S. was supported by a PhD. grant from the Fundação para a ciência e a Technologia, Programa Praxis XXI. J.C.S. and D.L.S. were supported by the MRC. This work was also supported by a Human Frontier Science Programme grant to J.C.S., S.W.W., H. Sive and N. Ueno. S.W.W. is a Wellcome Trust Senior Research Fellow supported by the BBSRC and the Wellcome Trust.
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Heisenberg, CP., Tada, M., Rauch, GJ. et al. Silberblick/Wnt11 mediates convergent extension movements during zebrafish gastrulation. Nature 405, 76–81 (2000). https://doi.org/10.1038/35011068
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DOI: https://doi.org/10.1038/35011068
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